Influence of activated A and B mating-type pathways on developmental processes in the basidiomycete Coprinus cinereus

Kües, Ursula; Pj, Walser; Mj, Klaus; Aebi, Markus

doi:10.1007/s00438-002-0745-7

Cited by 52 publications

(33 citation statements)

References 50 publications

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“…Expression of C. disseminatus genes in C. cinerea: C. cinerea monokaryon 218 (A3, B1, trp1.1,16, bad; Binninger et al 1987;Kü es et al 2002) was transformed according to the protocol given by Granado et al (1997). The trp1 1 vector pCc1001 (Binninger et al 1987) was used in cotransformations with plasmid pCR2.1-TOPO containing the entire Aa sublocus from strains TJ00/99.1 and TJ01/16.3 (plasmids 99.1Aa and 16.3Aa) and the entire Ab sublocus from strains TJ00/99.1 and TJ00/89.2 (99.1Ab and 89.2Ab).…”

Section: Methodsmentioning

confidence: 99%

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

et al. 2006

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Mating incompatibility in mushroom fungi is controlled by the mating-type loci. In tetrapolar species, two unlinked mating-type loci exist (A and B), whereas in bipolar species there is only one locus. The A and B mating-type loci encode homeodomain transcription factors and pheromones and pheromone receptors, respectively. Most mushroom species have a tetrapolar mating system, but numerous transitions to bipolar mating systems have occurred. Here we determined the genes controlling mating type in the bipolar mushroom Coprinellus disseminatus. Through positional cloning and degenerate PCR, we sequenced both the transcription factor and pheromone receptor mating-type gene homologs from C. disseminatus. Only the transcription factor genes segregate with mating type, discounting the hypothesis of genetic linkage between the A and B mating-type loci as the causal origin of bipolar mating behavior. The mating-type locus of C. disseminatus is similar to the A mating-type locus of the model species Coprinopsis cinerea and encodes two tightly linked pairs of homeodomain transcription factor genes. When transformed into C. cinerea, the C. disseminatus A and B homologs elicited sexual reactions like native matingtype genes. Although mating type in C. disseminatus is controlled by only the transcription factor genes, cellular functions appear to be conserved for both groups of genes. M ATING in fungi is controlled by the loci that determine the mating type of an individual, and only individuals with differing mating types can mate. Basidiomycete fungi have evolved a unique mating system, termed tetrapolar or bifactorial incompatibility, in which mating type is determined by two unlinked loci; compatibility at both loci is required for mating to occur. The origin of the tetrapolar mating system in the basidiomycetes is likely to be ancient since it is observed in at least two of the three major lineages, the Ustilaginomycetes, or smut fungi, and the Hymenomycetes, primarily the mushroom fungi (Burnett 1975). Also unique to the basidiomycetes is the presence of multiple alleles at the mating-type loci that allows most individuals within a population to be mating compatible with one another. Only the mushroom-forming homobasidiomycetes possess large allelic series at both loci, typically termed the A and B mating-type loci (Whitehouse 1949;Raper 1966).The multiallelic tetrapolar mating system is considered to be a novel innovation that could have only evolved once (Raper 1966;Raper and Flexer 1971). For this reason, the ancestor of the homobasidiomycetes is accepted as having a tetrapolar mating system. Although most (65%) of the homobasidiomycetes possess a tetrapolar mating system, many species (25%) instead have a bipolar system controlled by a single locus with multiple alleles (Raper 1966). The distribution of bipolar species is scattered throughout the homobasidiomycete phylogeny, and bipolar species appear to have multiple independent origins from tetrapolar mating systems (Hibbett and Donoghue 2001). The popul...

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Section: Methodsmentioning

confidence: 99%

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

et al. 2006

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“…So far, little is known about the genetic determinants that act in fruiting body initiation and formation. Induction of primary hyphal knots and the morphological transition from primary into secondary hyphal knots were shown to be regulated by the A and B mating-type genes (Kü es et al , 2002b. The gene pcc1, encoding an HMG-box transcription factor, likely acts downstream of the A mating-type gene products and appears to negatively regulate fruiting body initiation (Murata et al 1998).…”

Section: T He Heterothallic Fungus Coprinopsis Cinerea Servesmentioning

confidence: 99%

An Essential Gene for Fruiting Body Initiation in the Basidiomycete Coprinopsis cinerea Is Homologous to Bacterial Cyclopropane Fatty Acid Synthase Genes

et al. 2006

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The self-compatible Coprinopsis cinerea homokaryon AmutBmut produces fruiting bodies without prior mating to another strain. Early stages of fruiting body development include the dark-dependent formation of primary hyphal knots and their light-induced transition to the more compact secondary hyphal knots. The AmutBmut UV mutant 6-031 forms primary hyphal knots, but development arrests at the transition state by a recessive defect in the cfs1 gene, isolated from a cosmid library by mutant complementation. A normal primordia phenotype was achieved when cfs11 was embedded at both sides in at least 4.0 kb of native flanking DNA. Truncations of the flanking DNA lead to reduction in transformation frequencies and faults in primordia tissue formation, suggesting that the gene is also acting at later stages of development. The cfs1 gene encodes a protein highly similar to cyclopropane fatty acid synthases, a class of enzymes shown in prokaryotes and recently in a plant to convert membrane-bound unsaturated fatty acids into cyclopropane fatty acids. In C. cinerea 6-031, the mutant cfs1 allele carries a T-to-G transversion, leading to an amino acid substitution (Y441D) in a domain suggested to be involved in the catalytic function of the protein and/or membrane interaction.

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“…We believe that the most obvious explanation is that the developmental defects were a consequence of the cell cycle impairment. In C. cinerea developmental decisions are controlled by environmental conditions as well as by an appropriated balance of the mating-type regulators (Tymon et al 1992;Kües et al 1998Kües et al , 2002b. Therefore it seems likely that any condition affecting the correct dose of mating-type regulators will affect the further developmental decisions.…”

Section: Discussionmentioning

confidence: 99%

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

et al. 2013

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The fungal fruiting body or mushroom is a multicellular structure essential for sexual reproduction. It is composed of dikaryotic cells that contain one haploid nucleus from each mating partner sharing the same cytoplasm without undergoing nuclear fusion. In the mushroom, the pileus bears the hymenium, a layer of cells that includes the specialized basidia in which nuclear fusion, meiosis, and sporulation occur. Coprinopsis cinerea is a well-known model fungus used to study developmental processes associated with the formation of the fruiting body. Here we describe that knocking down the expression of Atr1 and Chk1, two kinases shown to be involved in the response to DNA damage in a number of eukaryotic organisms, dramatically impairs the ability to develop fruiting bodies in C. cinerea, as well as other developmental decisions such as sclerotia formation. These developmental defects correlated with the impairment in silenced strains to sustain an appropriated dikaryotic cell cycle. Dikaryotic cells in which chk1 or atr1 genes were silenced displayed a higher level of asynchronous mitosis and as a consequence aberrant cells carrying an unbalanced dose of nuclei. Since fruiting body initiation is dependent on the balanced mating-type regulator doses present in the dikaryon, we believe that the observed developmental defects were a consequence of the impaired cell cycle in the dikaryon. Our results suggest a connection between the DNA damage response cascade, cell cycle regulation, and developmental processes in this fungus. IN fungal cells, mating-the process equivalent to fertilizationbrings together two haploid nuclei in the same cytoplasm. It is generally thought that this process is essentially followed by nuclear fusion, resulting in a diploid nucleus that either enters meiosis immediately (as occurs in the fission yeast Schizosaccharomyces pombe) or is maintained and proliferates in the diploid state (as happens in the budding yeast Saccharomyces cerevisiae). However, in a large number of fungi, mating does not result in diploid nuclei. Instead, they form dikaryons, cells that contain one haploid nucleus from each mating partner sharing the same cytoplasm for a period of time without undergoing nuclear fusion or meiosis. These dikaryons continue to propagate, and eventually nuclear fusion will take place, which will be followed by meiosis, closing the sexual cycle (Brown and Casselton 2001).Dikaryon cell division, also called conjugate division, represents a big challenge to the cell since it has to ensure that each daughter dikaryon inherits a balance of each parental genome. For that, a complex cell cycle is required that involves distinct mechanisms to maintain heterokaryosis after cell division. For example, for a large number of Basidiomycota (e.g., the mushroom Coprinopsis cinerea), conjugate division includes the formation of a structure known as the clamp connection or clamp cell, as well as the sorting of one of the nuclei to this structure (Casselton 1978;Brown and Casselton 2001). In the...

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Influence of activated A and B mating-type pathways on developmental processes in the basidiomycete Coprinus cinereus

Cited by 52 publications

References 50 publications

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

Evolution of the Bipolar Mating System of the Mushroom Coprinellus disseminatus From Its Tetrapolar Ancestors Involves Loss of Mating-Type-Specific Pheromone Receptor Function

An Essential Gene for Fruiting Body Initiation in the Basidiomycete Coprinopsis cinerea Is Homologous to Bacterial Cyclopropane Fatty Acid Synthase Genes

A DNA Damage Checkpoint Pathway Coordinates the Division of Dikaryotic Cells in the Ink Cap MushroomCoprinopsis cinerea

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